War games in environmental bacteria

On the deeply intertwined evolutionary history between bacteria, their viruses, and an ever-growing arsenal of immune systems in complex microbial communities.
War games in environmental bacteria
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Viruses and bacteria are essential to life on Earth. For nearly 4 billion years, bacteria have co-evolved and faced relentless threats from specific viruses known as phages. The latter are the most abundant biological entities on Earth, with a number estimated at ~1031 viral particles in the biosphere1. Being greatly outnumbered, bacteria fend off phage assaults by deploying a multitude of innate and adaptive defense mechanisms like restriction-modification, abortive infection and CRISPR-Cas. Recent efforts to de-novo identify microbial defense systems resulted in the discovery of hundreds of additional innate immune mechanisms with a wide range of genetic architectures2,3, who have been precisely mapped across well-known reference genome databases4-6. While extremely insightful, such studies provide a limited snapshot of this bacterial defensome, as they miss the uncharted fraction of environmental microbial diversity that remains uncultured. This motivated us to build upon culture-independent genome-resolved metagenomics, and perform a large-scale in-depth investigation on the abundance, distribution, and diversity of the defensome in complex bacterial communities from three key environments: soil, marine, and human gut.

We found that the bacterial defensome is dramatically shaped by different ecological and geographical constraints. For example, we observed higher densities of defense systems in metagenome assembled genomes recovered from particularly challenging biomes such as serpentine soils or the arctic itself, in line with the high viral content described in such environments. We also observed that certain defense genes / systems favor different classes of mobile genetic elements presumably favoring their selfish spread, and that different associations are favored across distinct biomes. Interestingly, we found a preferential colocalization of subsets of families of defense systems inside defense islands, pointing for the possibility of previously unappreciated epistatic interactions. Finally, we identified a subset of defense genes having a higher-than-expected frequency of SNPs + indels, globally evolving under strong purifying selection, and a heterogeneous landscape of mutation types profoundly affected by the environment. Altogether, our work provides a first steppingstone toward identifying novel defense mechanisms in uncultivated microbes in complex microbial communities, to understand how such mechanisms collaborate or antagonize with one another, how they co-opt or are co-opted by mobile genetic elements, and how they are shaped by the surrounding environment.

Looking ahead, we think many questions are yet to be answered, particularly regarding how one can tackle the intricacies of these defense barriers in bacteria, with the purpose of developing more efficient phage-based therapeutics specifically targeting human and environmental pathogens of interest. Ultimately, we advocate that any clinical / environmental microbiome editing (e.g., in antibiotic replacement, microbiome grooming, etc) must be accompanied by a precise mapping of the metadefensome landscape followed by a rational design of the vector’s counter-defensome.

  1. Mushegian, A. R. Are there 1031 virus particles on Earth, or more, or fewer? J. Bacteriol. 202, e00052–20 (2020).
  2. Doron, S. et al. Systematic discovery of antiphage defense systems in the microbial pangenome. Science 359, eaar4120 (2018).
  3. Millman, A. et al. An expanded arsenal of immune systems that protect bacteria from phages. Cell Host Microbe 30, 1556–1569.e5 (2022).
  4. Tesson, F. et al. Systematic and quantitative view of the antiviral arsenal of prokaryotes. Commun. 13, 2561 (2022).
  5. Payne, L. J. et al. PADLOC: a web server for the identification of antiviral defence systems in microbial genomes. Nucleic Acids Res. 50, W541–W550 (2022).
  6. Oliveira, P. H., Touchon, M. & Rocha, E. P. C. The interplay of restriction-modification systems with mobile genetic elements and their prokaryotic hosts. Nucleic Acids Res. 42, 10618–10631 (2014).

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Comparative Genomics
Life Sciences > Biological Sciences > Genetics and Genomics > Genomics > Comparative Genomics
Environmental Microbiology
Life Sciences > Biological Sciences > Microbiology > Environmental Microbiology

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